Seasonal Effect of Gonadotrophin Inhibitory Hormone on Gonadotrophin-Releasing Hormone-induced Gonadotroph Functions in the Goldfish Pituitary

Journal of Neuroendocrinology

Volumn 25, Issue 5, 2013, Pages 506-516

  Moussavi, M ^a   Wlasichuk, M ^a,b   Chang, J P ^a,b   Habibi, H R ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Brain pituitary axis; GnIH receptor expression; Gonadotrophin inhibitory hormone and RF amides; Gonadotrophin production and secretion; Serum luteinising hormone

Indexed keywords

FOLLITROPIN BETA SUBUNIT; GONADORELIN; GONADOTROPHIN INHIBITORY HORMONE; HORMONE; LUTEINIZING HORMONE; LUTEINIZING HORMONE BETA SUBUNIT; MESSENGER RNA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GOLDFISH; HORMONE BLOOD LEVEL; HORMONE RECEPTOR INTERACTION; HYPOPHYSIS; HYPOPHYSIS CELL; LUTEINIZING HORMONE BLOOD LEVEL; LUTEINIZING HORMONE RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SEASONAL VARIATION;

ANIMALS; BASE SEQUENCE; DNA PRIMERS; FOLLICLE STIMULATING HORMONE; GOLDFISH; GONADOTROPIN-RELEASING HORMONE; GONADOTROPINS; LUTEINIZING HORMONE; PITUITARY GLAND; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEASONS;

EID: 84876344107     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/jne.12024     Document Type: Article

References (53)

1. Roch GJ, Busby ER, Sherwood NM. Evolution of GnRH: diving deeper. Gen Comp Endocrinol 2011; 171: 1-16.
2. Morgan K, Sellar R, Pawson AJ, Lu ZL, Millar RP. Bovine and ovine gonadotropin-releasing hormone (GnRH)-II ligand precursors and type II GnRH receptor genes are functionally inactivated. Endocrinology 2006; 147: 5941-5951.
3. Tsutsui K, Saigoh E, Ukena K, Teranishi H, Fujisawa Y, Kikuchi M, Ishii S, Sharp PJ. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochem Bioph Res Co 2000; 275: 661-667.
4. Sawada K, Ukena K, Satake H, Iwakoshi E, Minakata H, Tsutsui K. Novel fish hypothalamic neuropeptide. Eur J Biochem 2002; 269: 6000-6008.
5. Koda A, Ukena K, Teranishi H, Ohta S, Yamamoto K, Kikuyama S, Tsutsui K. A novel amphibian hypothalamic neuropeptide: isolation, localization, and biological activity. Endocrinology 2002; 143: 411-419.
6. Bentley GE, Perfito N, Ukena K, Tsutsui K, Wingfield JC. Gonadotropin-inhibitory peptide in song sparrows (Melospiza meodia) in different reproductive conditions, and in house sparrows (Passer domesticus) relative to chicken-gonadotropin-releasing hormone. J Neuroendocrinol 2003; 15: 794-802.
7. Osugi T, Ukena K, Bentley GE, O'Brien S, Moore IT, Wingfield JC, Tsutsui K. Gonadotropin-inhibitory hormone in Gambel's white-crowned sparrow (Zonotrichia leucophrys gamelii): cDNA identification, transcript localization and functional effects in laboratory and field experiments. J Endocrinol 2004; 182: 33-42.
8. Ciccone NA, Dunn IC, Boswell T, Tsutsui K, Ubuka T, Ukena K, Sharp PJ. Gonadotropin-inhibitory hormone depresses gonadotrophin alpha and follicle-stimulating hormone beta subunit expression in the pituitary of domestic chicken. J Neuroendocrinol 2004; 16: 999-1006.
9. Kriegsfeld LJ, Mei DF, Bentley GE, Ubuka T, Mason AO, Inoue K, Ukena K, Tsutsui K. Identification and characterizations of a gonadotropin-inhibitory system in the brains of mammals. Proc Natl Acad Sci USA 2006; 103: 2410-2415.
10. Ubuka T, Lai H, Kitani M, Suzuuchi A, Pham V, Cadigan PA, Wang A, Chowdhury VS, Tsutsui K, Bentley GE. Gonadotropin-inhibitory hormone identification, cDNA cloning, and distribution in rhesus macaque brain. J Comp Neurol 2009; 517: 841-855.
11. Sari IP, Rao A, Smith JT, Tilbrook AJ, Clarke IJ. Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology 2009; 150: 5549-5556.
12. Ubuka T, Morgan K, Pawson AJ, Osugi T, Chowdhury VS, Minakata H, Tsutsui K, Millar RP, Bentley GE. Identification of human GnIH homologs, RFRF-1 and RFRP-3, and the cognate receptor, GPR147 in the human hypothalamic pituitary axis. PLoS ONE 2009; 4: e8400.
13. Tsutsui K, Bentley GE, Bédécarrats G, Osugi T, Ubuka T, Kriegsfeld LJ. Gonadotropin-inhibitory hormone (GnIH) and its control of central and peripheral reproductive function. Front Neuroendocrin 2010; 31: 284-295.
14. Ubuka T, Kim S, Huang YC, Reid J, Jiang J, Osugi T, Chowdhury VS, Tsutsui K, Bentley GE. Gonadotropin-inhibitory hormone neurons interact directly with gonadotropin-releasing hormone-I and -II neurons in European starling brain. Endocrinology 2008; 149: 268-278.
15. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 2008; 149: 5770-5782.
16. Smith JT, Clarke IJ. Gonadotropin inhibitory hormone function in mammals. Trends Endocrin Met 2010; 21: 255-260.
17. Clarke IJ. Control of GnRH: one step back. Front Neuroendocrinol 2011; 32: 367-375.
18. Tsutsui K, Bentley GE, Kriegsfeld LJ, Osugi T, Seong JY, Vaudry H. Discovery and evolutionary history of gonadotropin-inhibitory hormone and kisspeptin: new key neuropeptides controlling reproduction. J Neuroendocrinol 2010; 22: 716-727.
19. Clarke IJ, Sari IP, Qi Y, Smith JT, Parkington HC, Ubuka T, Iqbal J, Li Q, Tilbrook A, Morgan K, Pawson AJ, Tsutsui K, Millar RP, Bentley GE. Potent action of RFamide-related peptide-3 on pituitary gonadotropes indicative of a hypophysiotropic role in the negative regulation of gonadotropin secretion. Endocrinology 2008; 149: 5811-5821.
20. Ducret E, Anderson GM, Herbison AE. RFamide-related peptide-3, a mammalian gonadotropin-inhibitory hormone orthologs, regulates gonadotropin-releasing hormone neuron firing in mouse. Endocrinology 2009; 150: 2799-2804.
21. Perfito N, Zann R, Ubuka T, Bentley G, Hau M. Potential roles for GNIH and GNRH-II in reproductive axis regulation of an opportunistically breeding songbird. Gen Comp Endocrinol 2011; 173: 20-26.
22. Yin H, Ukena K, Ubuka T, Tsutsui K. A novel G protein-coupled receptor for gonadotropin-inhibitory hormone in the Japanese quail (Coturnix japonica): identification, expression and binding activity. J Endocrinol 2005; 184: 257-266.
23. Maddineni S, Ocon-Grove OM, Krzysik-Walker SM, Hendricks GL III, Proudman JA, Ramachandran R. Gonadotrophin-inhibitory hormone receptor expression in the chicken pituitary gland: potential influence of sexual maturation and ovarian steroids. J Neuroendocrinol 2008; 20: 1078-1088.
24. Gibson EM, Humber SA, Jain S, Williams WP 3rd, Zhao S, Bentley GE, Tsutsui K, Kriegsfeld LJ. Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology 2008; 149: 4958-4969.
25. Zhang Y, Li S, Liu Y, Lu D, Chen H, Huang X, Liu X, Meng Z, Lin H, Cheng CHK. Structural diversity of the GnIH/GnIH receptor system in teleost: its involvement in early development and the negative control of LH release. Peptides 2010; 31: 1034-1043.
26. Moussavi M, Wlasichuk M, Chang JP, Habibi HR. Seasonal effect of GnIH on gonadotrope functions in the pituitary of goldfish. Mol Cell Endocrinol 2012; 350: 53-60.
27. Ikemoto T, Park MK. Chicken RFamide-related peptide (GnIH) and two distinct receptor subtypes: identification, molecular characterization, and evolutionary considerations. J Reprod Dev 2005; 51: 359-377.
28. Shimizu M, Bédécarrats GY. Activation of the chicken gonadotropin-inhibitory hormone receptor reduces gonadotropin releasing hormone receptor signaling. Gen Comp Endocrinol 2010; 167: 331-337.
29. Ubuka T, Ukena K, Sharp PJ, Bentley GE, Tsutsui K. Gonadotropin-inhibitory hormone inhibits gonadal development and maintenance by decreasing gonadotropin synthesis and release in male quail. Endocrinology 2006; 147: 1187-1194.
30. Son YL, Ubuka T, Millar RP, Kanasaki H, Tsutsui K. Gonadotropin-inhibitory hormone inhibits GnRH-induced gonadotropin subunit gene transcriptions by inhibiting AC/cAMP/PKA-dependent ERK pathway in LβT2 cells. Endocrinology 2012; 153: 2332-2343.
31. Amano M, Moriyama S, Ligo M, Kitamura S, Amiya N, Yamamori K, Ukena K, Tsutsui K. Novel fish hypothalamic neuropeptides stimulate the release of gonadotrophins and growth hormone form the pituitary of sockeye salmon. J Endocrinol 2006; 188: 417-423.
32. Yu KL, Rosenblum PM, Peter RE. In vitro release of gonadotropin-releasing hormone from the brain preoptic-anterior hypothalamic region and pituitary of female goldfish. Gen Comp Endocrinol 1991; 81: 256-267.
33. Omeljaniuk RJ, Habibi HR, Peter RE. Alterations in pituitary GnRH and dopamine receptors associated with the seasonal variation and regulation of gonadotropin release in the goldfish (Carassius auratus). Gen Comp Endocrinol 1989; 74: 392-399.
34. Peter RE, Nahorniak CS, Chang JP, Crim LW. Gonadotropin release from the pars distalis of goldfish, Carassius auratus, transplanted beside the brain or into brain ventricle: additional evidence for gonadotropin-release-inhibitory factor. Gen Comp Endocrinol 1984; 55: 337-346.
35. Chang JP, Cook H, Freedman GL, Wiggs AJ, Somoza GM, de Leeuw R, Peter RE. Use of a pituitary cell dispersion method and primary culture system for the studies of gonadotropin-releasing hormone action in the goldfish, Carassius auratus. I. Initial morphological, static, and cell column perifusion studies. Gen Comp Endocrinol 1990; 77: 256-273.
36. Wong AOL, Chang JP, Peter RE. Dopamine stimulates growth hormone release from the pituitary of goldfish, Carassius auratus, through the dopamine D1 receptors. Endocrinology 1992; 130: 1201-1210.
37. Sawisky GR, Chang JP. Intracellular calcium involvement in pituitary adenylate cyclase-activating polypeptide stimulation of growth hormone and gonadotropin secretion in goldfish pituitary cells. J Neuroendocrinol 2005; 17: 353-371.
38. Trudeau VL, Peter RE, Sloley BD. Testosterone and estradiol potential the serum gonadotropin response to gonadotropin-releasing hormone in goldfish. Biol Reprod 1991; 44: 951-960.
39. Pasmanik M, Callard GV. Changes in brain aromatase and 5 alpha-reductase activities correlated significantly with seasonal reproductive cycles in goldfish (Carassius auratus). Endocrinology 1988; 122: 1349-1356.
40. Habibi HR, Marchant TA, Nahorniak CS, Van Der Loo H, Peter RE, Rivier JE, Vale WW. Functional relationship between receptor binding and biological activity for analogs of mammalian and salmon gonadotropin-releasing hormones in the pituitary of goldfish (Carassius auratus). Biol Reprod 1989; 40: 1152-1161.
41. Ubuka T, Inoue K, Fukuda Y, Mizuno T, Ukena K, Kriegsfeld LJ, Tsutsui K. Identification, expression, and physiological functions of Siberian hamster gonadotropin-inhibitory hormone. Endocrinology 2012; 153: 373-385.
42. Chang JP, Van Goor F, Neumann CM. Interactions between protein kinase C and arachidonic acid in the gonadotropin response to salmon and chicken gonadotropin-releasing hormone-II in goldfish. Gen Comp Endocrinol 1994; 93: 304-320.
43. Jobin RM, Neumann CM, Chang JP. Roles of calcium and calmodulin in the mediation of acute and sustained GnRH-stimulated gonadotropin secretion from dispersed goldfish pituitary cells. Gen Comp Endocrinol 1996; 101: 91-106.
44. Billiard J, Koh DS, Babcock DF, Hille B. Protein kinase C as a signal of exocytosis. Proc Natl Acad Sci USA 1997; 94: 12192-12197.
45. Martin TF. Tuning exocytosis for speed: fast and slow modes. Biochim Biophys Acta 2003; 1641: 157-165.
46. Chang JP, Johnson JD, Van Goor F, Wong CJ, Yunker WK, Uretsky AD, Taylor D, Jobin RM, Wong AO, Goldberg JL. Signal transduction mechanisms mediating secretion in goldfish gonadotropes and somatotropes. Biochem Cell Biol 2000; 78: 139-153.
47. Chang JP, Johnson JD, Sawisky GR, Grey CL, Mitchell G, Booth M, Volk MM, Parks SK, Thomspon E, Goss GG, Klausen C, Habibi HR. Signal transduction in multifactorial neuroendocrine control of gonadotropin secretion and synthesis in teleosts-studies on the goldfish model. Gen Comp Endocrinol 2009; 161: 42-52.
48. Khakoo Z, Bhatia A, Gedamu L, Habibi HR. Functional specificity for salmon gonadotropin-releasing hormone (GnRH) and chicken GnRH-II coupled to the gonadotropin release and subunit messenger ribonucleic acid level in the goldfish pituitary. Endocrinology 1994; 134: 838-847.
49. Klausen C, Chang JP, Habibi HR. Time- and dose-related effects of gonadotropin-releasing hormone on growth hormone and gonadotropin subunit gene expression in the goldfish pituitary. Can J Physiol Pharm 2002; 80: 915-924.
50. Coss D, Hand CM, Yaphockun KK, Ely HA, Mellon PL. p38 mitogen-activated kinase is critical for synergistic induction of the FSH beta gene by gonadotropin-releasing hormone and activin through augmentation of c-Fos induction and Smad phosphorylation. Mol Endocrinol 2007; 21: 3071-3086.
51. Naor Z, Jabbour HN, Naidich M, Pawson AJ, Morgan K, Battersby S, Millar MR, Brown P, Millar RP. Reciprocal cross talk between gonadotropin-releasing hormone (GnRH) and prostaglandin receptors regulates GnRH receptor expression and differential gonadotropin secretion. Mol Endocrinol 2007; 21: 527-537.
52. Klausen C, Chang JP, Habibi HR. Multiplicity of gonadotropin-releasing hormone signaling: a comparative perspective. Prog Brain Res 2002; 141: 111-128.
53. Shahjahan M, Ikegami T, Osugi T, Ukena K, Doi H, Hattori A, Tsutsui K, Ando H. Syncronised expressions of LPXRFamide peptide and its receptor genes: seasonal, diurnal and circadian changes during spawning period in grass puffer. J Neuroendocrinol 2011; 23: 39-51.